Developmental expression of BMP4\ALK3\SMAD5 signaling pathway in the mouse testis: A potential role of BMP4 in spermatogonia differentiation

Journal of Cell Science

Volumn 116, Issue 16, 2003, Pages 3363-3372

  Pellegrini, Manuela ^a   Grimaldi, Paola ^a   Rossi, Pellegrino ^a   Geremia, Raffaele ^a   Dolci, Susanna ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Alk3; BMP4; Kit; Smad5; Spermatogonia

Indexed keywords

ALK3 PROTEIN; BONE MORPHOGENETIC PROTEIN 4; PROTEIN P300; RECEPTOR PROTEIN; SMAD PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; STEM CELL FACTOR; THYMIDINE; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; DOWN REGULATION; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PREPUBERTY; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SENSITIVITY ANALYSIS; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL; TESTIS DEVELOPMENT; TRANSCRIPTION INITIATION;

ACETYLTRANSFERASES; ACTIVIN RECEPTORS; ANIMALS; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HISTONE ACETYLTRANSFERASES; MALE; MICE; MICROSCOPY, FLUORESCENCE; PHOSPHOPROTEINS; PROTO-ONCOGENE PROTEINS C-KIT; SERTOLI CELLS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; SMAD5 PROTEIN; SPERMATOGENESIS; SPERMATOGONIA; TESTIS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0042386233     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00650     Document Type: Review

References (49)

1. Blume-Jensen, P., Jiang, G., Hyman, R., Lee, K. F, O'Gorman, S. and Hunter, T. (2000). Kit/stem cell factor receptor-induced activation of phosphatidylinositol 3′-kinase is essential for male fertility. Nat. Genet. 24, 157-162.
2. Brannan, C. I, Bedell, M. A., Resnick, J. L., Eppig, J. J., Handel, M. A., Williams, D. E., Lyman, S. D., Donovan, P. J., Jenkins, N. A. and Copeland, N. G. (1992). Developmental abnormalities in Steel171H mice result from a splicing defect in the steel factor cytoplasmic tail. Genes Dev. 6, 1832-1842.
3. Chang, H. and Matzuk, M. (2001). Smad5 is required for mouse primordial germ cell development. Mech. Dev. 104, 61-67.
4. De Caestecker, M. P., Yahata, T., Wang, D., Parks, W. T., Huang, S., Hill, C. S., Shioda, T., Roberts, A. B. and Lechleider, R. J. (2000). The Smad4 activation domain (SAD) is a proline-rich, p300-dependent: transcriptional activation domain. J. Biol. Chem. 275, 2115-2122.
5. De Rooij, D. G. (2001). Proliferation and differentiation of spermatogonial stem cells. Reproduction 121, 347-354.
6. Dolci, S., Williams, D. E., Ernst, M. K., Resnick, J. L., Brannan, C. I, Lock, L. F., Lyman, S. D., Boswell, H. S. and Donovan, P. J. (1991). Requirement for mast cell growth factor for primordial germ cell survival in culture. Nature 352, 809-811.
7. Dolci, S., Pellegrini, M., di Agostino, S., Geremia, R. and Rossi, P. (2001). Signaling through extracellular signal-regulated kinase is required for spermatogonial proliferative response to stem cell factor. J. Biol. Chem. 276, 40225-40233.
8. Feng, X. H., Zhang, Y., Wu, R. Y. and Derynck, R. (1998). The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for smad3 in TGF-beta-induced transcriptional activation. Genes Dev. 12, 2153-2163.
9. Feng, L. X., Ravindranath, N. and Dym, M. (2000). Stem cell factor/c-kit up-regulates cyclin D3 and promotes cell cycle progression via the phosphoinositide 3-kinase/p7O S6 kinase pathway in spermatogonia. J. Biol. Chem. 275, 25572-25576.
10. Fujiwara, T., Dunn, N. R. and Hogan, B. L. (2001). Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse. Proc. Natl. Acad. Sci. USA 98, 13739-13744.
11. Graff, J. M., Bansal, A. and Melton, D. A. (1996). Xenopus Mad proteins transduce distinct subsets of signals for the TGF beta superfamily. Cell 85, 479-487.
12. Grimaldi, P., Piscitelli, D., Albanesi, C., Blasi, F., Geremia, R. and Rossi, P. (1993). Identification of 3′,5cyclic adenosine monophosphate-inducible nuclear factors binding to the human urokinase promoter in mouse Sertoli cells. Mol. Endocrinol. 7, 1217-1225.
13. Heinrich, M. C., Dooley, D. C. and Keeble, W. W. (1995). Transforming growth factor beta 1 inhibits expression of the gene products for steel factor and its receptor (c-kit). Blood 85, 1769-1780.
14. Heldin, C. H., Miyazono, K. and ten Dijke, P. (1997). TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
15. Hoodless, P. A., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M. B., Attisano, L. and Wrana J. L. (1996). MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
16. Ishida, W., Hamamoto, T., Kusanagi, K., Yagi, K., Kawabata, M., Takehara, K., Sampath, T. K., Kato, M. and Miyazono, K. (2000). Smad6 is a Smad1/5-induced smad inhibitor. Characterization of bone morphogenetic protein-responsive element in the mouse Smad6 promoter. J. Biol. Chem. 275, 6075-6079.
17. Janknecht, R., Wells, N. J. and Hunter, T. (1998). TGF-beta-stimulated cooperation of smad proteins with the coactivators CBP/p300. Genes Dev. 12, 2114-2119.
18. Kawakami, T., Soma, Y., Kawa, Y., Ito, M., Yamasaki, E., Watabe, H., Hosaka, E., Yajima, K., Ohsumi, K. and Mizoguchi, M. (2002). Transforming growth factor beta1 regulates melanocyte proliferation and differentiation in mouse neural crest cells via stem cell factor/KIT signaling. J. Invest. Dermatol. 118, 471-478.
19. Kim, J., Johnson, K., Chen, H. J., Carroll, S. and Laughon, A. (1997). Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388, 304-308.
20. Kissel, H., Timokhina, I, Hardy, M. P., Rotschild, G., Tajima, Y., Soares, V., Angeles, M., Whitlow, S. R., Manova, K. and Bessmer P. (2000). Point mutation in Kit receptor tyrosine kinase reveals essential roles for kit signaling in oogenesis and spermatogenesis without affecting other kit responses. EMBO J. 19, 1312-1326.
21. Kusanagi, K., Inoue, H., Ishidou, Y., Mishima, H. K., Kawabata, M. and Miyazono, K. (2000). Characterization of a bone morphogenetic protein-responsive Smad-binding element. Mol. Biol. Cell 11, 555-565.
22. Krosl, G., He, G., Lefrancois, M., Charron, F., Romeo, P. H., Jolicoeur, P., Kirsch, I. R., Nemer, M. and Hoang, T. (1998). Transcription factor SCL is required for c-kit expression anq c-Kit function in hemopoietic cells. J. Exp. Med.-188, 439-450.
23. Lawson, K. A., Dunn, N. R., Roelen, B. A., Zeinstra, L. M., Davis, A. M., Wright, C. V., Korving, J. P. and Hogan, B. L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-436.
24. Mannervik, M. and Akusjarvi, G. (1997). The transcriptional co-activator proteins p300 and CBP stimulate adenovirus E1A conserved region 1 transactivation independent of a direct interaction. FEBS Lett. 414, 111-116.
25. Manova, K., Nocka, K., Besmer, P. and Bachvarova, R. F. (1990). Gonadal expression of c-kit encoded at the W locus of the mouse. Development 110, 1057-1069.
26. Meng, X., Lindahl, M., Hyvonen, M. E., Parvinen, M., de Rooij, D. G., Hess, M. W., Raatikainen-Ahokas, A., Sainio, K., Rauvala, H., Lakso, M. et al. (2000). Regulation of cell fate decision of undifferentiated spermatogonia by GDNF Science 287, 1489-1493.
27. Nishihara, A., Hanai, J. I., Okamoto, N., Yanagisawa, J., Kato, S., Miyazono, K. and Kawabata, M. (1998). Role of p300, a transcriptional coactivator, in signalling of TGF-beta. Genes Cells 3, 613-623.
28. Nishimura, R., Kato, Y., Chen, D., Harris, S. E., Mundy, G. R. and Yoneda, T. (1998). Smad5 and DPC4 are key molecules in mediating BMP-2-induced osteoblastic differentiation of the pluripotent mesenchymal precursor cell line C2C12. J. Biol. Chem. 273, 1872-1879.
29. Pesce, M., Klinger, G. F. and de Felici, M. (2002). Derivation in culture of primordial germ cells from cells of the mouse epiblast: phenotypic induction and growth control by Bmp4 signalling. Mech. Dev. 112, 15-24.
30. Pouponnot, C., Jayaraman, L. and Massague, J. (1998). Physical and functional interaction of SMADs and p300/CBP. J. Biol. Chem. 273, 22865-22868.
31. Rossi, P., Albanesi, C., Grimaldi, P. and Geremia, R. (1991). Expression of the mRNA for the ligand of c-kit in mouse sertoli cells. Biochem. Biophys. Res. Commun. 176, 910-914.
32. Rossi, P., Marziali, G., Albanesi, C., Charlesworth, A., Geremia, R. and Sorrentino, V. (1992). A novel c-kit transcript, potentially encoding a truncated receptor, originates within a kit gene intron in mouse spermatids. Dev. Biol. 152, 203-207.
33. Rossi, P., Dolci, S., Albanesi, C., Grimaldi, P., Ricca, R. and Geremia, R. (1993). Follicle-stimulating hormone induction of steel factor (SLF) mRNA in mouse sertoli cells and stimulation of DNA synthesis in spermatogonia by soluble SLF. Dev. Biol. 155, 68-74.
34. Sansilvestri, P., Cardoso, A. A., Batard, P., Panterne, B., Hatzfeld, A., Lim, B., Levesque, P., Monier, M. N. and Hatzfeld, J. (1995). Early CD34high cells can be separated into KIT high cells in which transforming growth factor-beta (TGF-beta) downmodulates c-kit and KIT low cells in which anti-TGF-beta upmodulates c-kit. Blood 86, 1729-1735.
35. Schrans-Stassen, B. H., van de Kant, H. J., de Rooij, D. G. and van Pelt, A. M. (1999). Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 140, 5894-5900.
36. Sorrentino, V., Giorgi, M., Geremia, R., Besmer, P. and Rossi, P. (1991). Expression of the c-kit proto-oncogene in the murine male germ cells. Oncogene 6, 149-151.
37. Tomeczkowski, J., Frick, D., Schwinzer, B., Wittner, N., Ludwig, W. D., Reiter, A., Welte, K. and Sykora, K. W. (1998). Expression and regulation of c-kit receptor and response to stem cell factor in childhood malignant T- lymphoblastic cells. Leukemia 12, 1221-1229.
38. Topper, J. N., DiChiara, M. R., Brown, J. D., Williams, A. J., Falb, D., Collins, T. and Gimbrone, M. A. Jr (1998). CREB binding protein is a required coactivator for Smad-dependent, transforming growth factor beta transcriptional responses in endothelial cells. Proc. Natl. Acad. Sci. USA 95, 9506-9511.
39. Tremblay, K. D., Dunn, N. R. and Robertson, E. J. (2001). Mouse embryos lacking Smadl signals display defects in extra-embryonic tissues and germ cell formation. Development 128, 3609-3621.
40. Tsujimura, T., Morii, E., Nozaki, M., Hashimoto, K., Moriyama, Y., Takebayashi, K., Kondo, T., Kanakura, Y. and Kitamura, Y. (1996). Involvement of transcription factor encoded by the mi locus in the expression of c-kit receptor tyrosine kinase in cultured mast cells of mice. Blood 88, 1225-1233.
41. Viglietto, G., Dolci, S., Bruni, P., Baldassarre, G., Chiariotti, L., Melillo, R. M., Salvatore G., Chiappetta, G., Sferratore, F., Fusco, A. and Santoro, M. (2000). Glial cell line-derived neutrotrophic factor and neurturin can act as paracrine growth factors stimulating DNA synthesis of Ret-expressing spermatogonia. Int. J. Oncol. 16, 689-694.
42. Xu, X., Yin, Z., Hudson, J. B., Ferguson, E. L. and Frasch, M. (1998). Smad proteins act in combination with synergistic and antagonistic regulators to target Dpp responses to the Drosophila mesoderm. Genes Dev. 12, 2354-2370.
43. Ying, Y., Liu, X. M., Marble, A., Lawson, K. A. and Zhao, G. Q. (2000). Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol. Endocrinol. 14, 1053-1063.
44. Ying, Y. and Zhao, G. Q. (2001) Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 232, 484-492.
45. Ying, Y., Qi, X. and Zhao, G. Q. (2001). Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc. Natl. Acad. Sci. USA 98, 7858-7862.
46. Yoshinaga, K., Nishikawa, S., Ogawa, M., Hayashi, S., Kunisada, T., Fujimoto, T. and Nishikawa, S. (1991). Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113, 689-699.
47. Zhang, Y., Musci, T. and Derynck, R. (1997). The tumor suppressor Smad4/DPC 4 as a central mediator of Smad function. Curr. Biol. 7, 270-276.
48. Zhao, G. Q., Deng, K., Labosky, P. A., Liaw, L. and Hogan, B. L. (1996). The gene encoding bone morphogenetic protein 8B is required for the initiation and maintenance of spermatogenesis in the mouse. Genes Dev. 10, 1657-1669.
49. Zhao, G. Q. and Hogan, B. L. (1997). Evidence that Mothers-against-dpp-related 1 (Madr1) plays a role in the initiation and maintenance of spermatogenesis in the mouse. Mech. Dev. 61, 63-73.